Multi-omic investigation to decipher host-microbiota relationships in dairy cattle in the context of methane inhibition
Résumé
Ruminants emit substantial amounts of methane, a potent greenhouse gas, during feed fermentation. It is not only an environmental threat but also a useless conversion of feed energy for the host. To date, direct inhibition of methanogenesis by specific additives is a successful mitigation strategy but is not associated with energy gain for the host. The objective of this study is to understand the microbiota-host relationship during methanogenesis inhibition to bring out hypothesis on the fate of energy when methane production is inhibited. Twenty-five Holstein cows were fed the same diet with or without the methyl-coenzyme M reductase inhibitor 3-nitrooxypropanol (3-NOP) for six weeks. Plasma was used to assess the host metabolome and rumen juice was used to investigate microbial taxonomy and gene expression by metagenomics and metatranscriptomics. In order to disentangle differences in expression related to differences in microbial abundance, a preliminary normalization step was performed to account for gene abundance. Normalized transcripts and microbial taxonomy were used as explanatory blocks into a multi-block sparse partial least square regression (MB-sPLS) to explain the block of plasma metabolites variation. Features selected by the MB-sPLS were mapped as a correlative network. In the 3-NOP group, the one-carbon metabolism amino acids serine, glycine, and methionine increased and held high centrality positions in the network. The rumen taxa of the network were mostly from the Acutalibacteraceae family. Normalized transcripts which also composed the network included downregulated transcripts of methanogenesis (methyl-coenzyme M reductase, ferredoxin), glycolysis (glyceride-3-phosphate dehydrogenase, pyruvate phosphate dikinase) and microbial protein synthesis (elongation factors). These results emphasize the interplay between methyl compound transfer from microbial glycolysis and methanogenesis and one-carbon metabolism in the host. Perturbation of microbial glycolysis combined with stimulation of non-energetic metabolic pathway in the host may explain why methane inhibition is not associated with enhanced energy gain for the host.